Analysis of ontogenetic changes in head shape and diet in a with moderately enlarged jaw adductors (Clariallabes melas) Marisa Wyckmans, Anthony Herrel, Dominique Adriaens

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Marisa Wyckmans, Anthony Herrel, Dominique Adriaens. Analysis of ontogenetic changes in head shape and diet in a catfish with moderately enlarged jaw adductors (Clariallabes melas). Belgian Journal of Zoology, Royal Belgian Zoological Society, 2011, 141 (2), pp.11-20. ￿hal-02436104￿

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HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Belg. J. Zool., 141 (2) : 11-20 July 2011

Analysis of ontogenetic changes in head shape and diet in a catfish with moderately enlarged jaw adductors (Clariallabes melas)

Marisa Wyckmans1, Anthony Herrel2* & Dominique Adriaens3

1 Dept. Biology, University of Antwerp, Universiteitsplein 1, B-2610 Antwerpen, Belgium. E-mail: [email protected] 2 Dept. d’Ecologie et Gestion de la Biodiversité, Muséum National d’Histoire Naturelle, 57 rue Cuvier, 75231, Paris, France. E-mail: [email protected] 3 Dept. Biology, Ghent University, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium. E-mail: [email protected]

* Corresponding author: [email protected]

ABSTRACT. Jaw adductor hypertrophy, or the presence of enlarged jaw-closing muscles, has arisen several times independently in African clariid catfish. Previous work has demonstrated that species characterized by enlarged jaw adductors may have unusual ways of foraging such as terrestrial foraging and prey capture, and often include a large proportion of hard and terrestrial prey in their diet. However, relatively little is known about species of the Clariallabes with an intermediate degree of jaw adductor hypertrophy. In the present study we present data on head shape and diet for a range of sizes of specimens of a poorly known species of Clariallabes, C. melas. Our data show that growth patterns in this species and the previously studied C. longicauda are similar in some ways (e.g. positive allometry of the growth of the jaw muscles) but different in others (negative allometry in hyoid width). However, C. melas has a smaller head for its body size in all dimensions. Due to the large number of empty stomachs we encountered, dietary data remain preliminary, but suggest a varied diet including both hard and soft prey. Our data show that a large amount of variation in head shape may exist even among related species and that species with jaw adductor hypertrophy generally show positive allometry in the growth of the jaw adductors and associated structures. Whether jaw muscle hypertrophy is an adaptive trait in clariid catfish awaits further comparative analyses testing for the evolutionary association between jaw adductor hypertrophy and the inclusion of hard prey into the diet.

Key words: fish, muscle, biting, suction, feeding, ontogeny

INTRODUCTION (Lauder, 1983; Korff & Wainwright, 2004). Interestingly, hypertrophy of the jaw adductors In fish, the inclusion of hard prey into the diet is often noted in populations showing a higher (durophagy) is often associated with changes proportion of molluscs in the diet, suggesting in dentition (e.g. Streelman & Albertson, an adaptive evolutionary response of the cranial 2006), the presence of enlarged pharyngeal morphology to diet (Turingan et al., 1995). or oral jaw adductor muscles (Wainwright, Moreover, a strong plastic response in muscle 1987; Hernandez & Motta, 1997), an size to an increase of molluscs in the diet has overall increase in the robustness of the oral been demonstrated in some fish M( ittelbach et or pharyngeal jaws and the skull (Cabuy et al., 1999). al., 1999; Grubich, 2003) and in some species durophagy is associated with the presence Oral jaw adductor hypertrophy has arisen of a specialized muscle activation pattern several times independently in African clariid 12 Marisa Wyckmans, Anthony Herrel & Dominique Adriaens

catfish (Jansen et al., 2006; Devaere et al., Wassenbergh et al., 2006a), and that they 2007). Indeed, a recent study using combined include a large proportion of hard and often morphological and molecular data suggests that terrestrial prey in their diet (Huysentruyt an increase in jaw adductor size has originated at et al., 2004). However, the species with least four times independently (Devaere et al., the most extreme degree of jaw adductor 2007). Clariid catfish are, however, not known hypertrophy appear to swallow their prey to be mollusc crushers and retain large pointed whole (Huysentruyt et al., 2004). Previous teeth on the jaws (Devaere et al., 2001). Among studies have shown that rapidly-growing and clariid catfish species, jaw adductor hypertrophy suction-feeding clariid species, such as Clarias ranges from the normal dorsoventrally- gariepinus grow isometrically (Herrel et al., compressed type with the jaw adductors largely 2005). In contrast, the growth of jaw adductors covered by the cranial bones (e.g. within the and related structures shows positive allometry genus Clarias), to a situation where most of the in a species with an intermediate degree of jaw dorso-lateral cranial bones are strongly reduced hypertrophy, such as Clariallabes longicauda to make space for the jaw adductor muscles (Wykmans et al., 2007). In order to test the (e.g. within the genus Channallabes) (Devaere hypothesis that species with intermediate degrees et al., 2001). Although the species with more of jaw hypertrophy are characterised by positive pronounced degrees of jaw adductor hypertrophy allometric growth, we analysed growth patterns have been relatively well studied, little is known in a species with an intermediate degree of jaw about species with an intermediate degree of jaw adductor hypertrophy (Clariallabes melas; adductor hypertrophy, such as those of the genus Boulenger 1887). Moreover we compare Clariallabes (but see Wyckmans et al., 2007). patterns of growth in C. melas to those observed for its congener, C. longicauda (Boulenger, In other vertebrates, an increase in the size of the 1902) and present data on diet for a range of oral jaw adductor muscles is typically associated sizes of individuals of C. melas. with an increase in bite force (Herrel et al., 2007a), and in many vertebrates an increase in bite force is associated with the inclusion of MATERIALS AND METHODS hard or large prey into the diet (Herrel et al., 2002; Aguirre et al., 2003; Herrel et al., 2005; Material examined Huber et al., 2009). However, at least for some groups such as lizards, it has been shown that The 51 Clariallabes melas used in this study sexual selection for increased fighting capacity were obtained from the Royal Museum for may also lead to increased bite force (Lailvaux Central Africa (RMCA - KMMA), Tervuren, et al., 2004; Huyghe et al., 2005; Lappin & Belgium. All specimens (30592-603-1 to 10; Husak, 2005) and sexual differences in the size 68800-68802-1 to 2; 117776-117780-1 to 5; of the jaw adductors (Herrel et al., 2007b). 119100-101-1 to 2; 29660; 46746-46747-1 to Moreover, in some burrowing mammals, high 2; 117770-117775-1 to 2; 178220-230-MEL15, bite force may be associated with the ability to 178220-230-1; 19072-19074-1; 38495-38508-1 dig tunnels into hard soils rather than diet (Van to 2; 44916-917-1 to 2; 74381; 79220; 96646- Daele et al., 2009) suggesting that a multitude 96648-1 to 2; 98931; 119117; 138665; 73-68-P- of selective pressures may be operating on jaw 566-574-1 to 8; 86-06-P-51-53-1 to 2; 88-01-P- muscle size and bite force capacity. 1993; 88-01-P-1994-1995-1 to 2) were collected in the Congo River drainage. Fish included in Previous work on clariid catfish with enlarged this study range from 116 to 329mm total length oral jaw adductors has demonstrated that and encompass juvenile (i.e. non-reproductive) some of these species have unusual ways of and adult specimens. foraging including terrestrial prey capture (Van Head shape and diet in Clarriallabes 13

Morphometrics greater degree, they should be more successful in capturing elusive prey. Body size (both total length and standard length) and head dimensions were measured Diet using digital calipers (Mitutoyo CD-30C and CD- 15B; ± 0.01mm). Head length was measured as Stomach contents were removed in situ through the distance between the tip of the snout and the a ventral incision, and preserved in a 70% aqueous caudal edge of the occipital process. Head width ethanol solution. All prey items were sorted and and head height were measured just posterior to identified using a binocular microscope (Wild the jaw adductors. M3Z). Because the majority of organisms found in the stomachs were crushed and/or digested, The surface area taken up by the jaw adductors they were identified to the level of order or higher in dorsal view was determined using digital taxonomic level where appropriate. photographs of each specimen and is used here as a proxy for jaw adductor size (see Fig. 1; The number of prey items found in every Wyckmans et al., 2007). For our analyses, the stomach was counted and for every prey item average of the left and right sides was calculated. prey size was estimated. Intact prey items were Additionally the maximal width of the head and measured using digital calipers (Mitutoyo CD- the width of the neurocranium were determined 15B; ± 0.01mm). Non-intact prey items were on these pictures. Measurements were carried grouped in size classes, from 0–45mm, at 5mm out using tpsDIG (version 1.40; Rohlf, 2004). intervals. Average prey size, maximal prey size A scale bar (1mm grid) was included in each and the proportion of large prey (i.e. > 20mm) photograph, allowing us to convert pixel consumed were calculated for each individual measurements to metric units. These measures fish. In addition, every prey group was weighed were taken as previous studies have shown using an electronic microbalance (Mettler Toledo them to be correlated with the inclusion of MT5; ± 0.001mg). For each prey group, a relative functionally-different prey into the diet in fish importance index (IRI) was calculated as an (Wyckmans et al., 2007). indicator of the significance of that particular prey group in the diet (Huysentruyt et al., 2004): To determine the dimensions of a number of IRI=(%N+%V)× %Oc where %N and %Oc internal skeletal elements, X-ray photographs are, respectively, the numeric abundance and (dorsoventral view) were made using a Philips the frequency of occurrence of a particular prey Optimus X-ray unit with image intensifier, group. %V is the mass that particular prey group coupled to a Redlake Imaging MotionPro contributes to total prey mass. In addition, %IRI high resolution digital video camera. On each was calculated, being the proportion of IRI of photograph eight landmarks were digitized using each prey group in relation to the total IRI value. Didge (version 2.2.0.; Cullum A.). Based on the X-Y coordinates, the length and width of the Statistical analysis lower jaw and the hyoid, the length of the hyoid bars, the angle between the two hyoid bars and the To investigate size-related changes in width of the pectoral girdle were calculated (see morphology, log10 transformed morphological

Fig. 2; Wyckmans et al., 2007). These measures measures were regressed against the log10 are thought to reflect the ability of these fish to transformed standard length. A two-tailed enlarge the oral cavity and thus their ability to Student t-test was used to test for differences capture elusive prey (Van Wassenberg et al., between the observed slopes obtained from the 2006c;d). As fish having wider pectoral girdles regression analyses and the slopes expected in and longer and wider hyoids should be able the case of isometric growth (Sokal & Rohlf, to increase the volume of the oral cavity to a 1995). Isometry is the expected mode of growth 14 Marisa Wyckmans, Anthony Herrel & Dominique Adriaens for ectotherms growing throughout their life of isometric growth. Whereas jaw adductor size and has been demonstrated for non-specialized (Student t-test, d.f.=50, t=2.02, 0.02

Clariallabes melas versus C. longicauda RESULTS Significant interspecific differences were Ontogenetic changes in head size and shape detected for all morphological traits examined. in Clariallabes melas Taking into account the observed difference in average body size (SL) (one-way ANOVA;

All morphological traits examined are F1,105=10.36; p=0.002), it is clear that C. correlated with fish body size (all R²>0.120 and longicauda, despite its smaller body size has p<0.016; Table 1). The observed ontogenetic a broader, more robust head and larger jaw changes in morphology, however, were not adductor muscles than does C. melas (ANCOVA; always consistent with those expected for a model all p<0.002; see Fig. 1).

TABLE 1 Table summarizing the scaling of head dimensions relative to body size in Clariallabes melas. d.f. = degrees of freedom; S.E. = standard error of the slope.

EXPECTED OBSERVED S.E. d.f. t P SLOPE SLOPE Total length (mm) 1 0.990 0.010 50 -1.000 0.30 < P < 0.50 Cranial length (mm) 1 0.940 0.056 50 -1.071 0.20 < P < 0.30 Cranial width (mm) 1 1.005 0.057 45 0.088 > 0.90 Cranial depth (mm) 1 1.011 0.066 50 0.167 0.80 < P < 0.90 Neurocranial width (mm) 1 0.802 0.099 50 -2.000 0.05 < P < 0.10 Head width (mm) 1 1.005 0.067 47 0.075 > 0.90 Surface area jaw adductors (mm2) 2 2.269 0.133 50 2.023 0.02 < P < 0.05 Width lower jaw (mm) 1 0.879 0.047 50 -2.574 0.01 < P < 0.02 Length lower jaw (mm) 1 0.978 0.063 50 -0.349 0.70 < P < 0.80 Width hyoid (mm) 1 0.883 0.048 47 -2.438 0.01 < P < 0.02 Length hyoid (mm) 1 1.111 0.088 47 1.261 0.20 < P < 0.30 Hyoid angle (°) 0 -0.149 0.060 47 -2.483 0.01 < P < 0.02 Width pectoral girdle (mm) 1 0.959 0.061 48 -0.672 0.50 < P < 0.70 Head shape and diet in Clarriallabes 15

TABLE 2 Table summarizing the diet of Clariallabes melas. Occurrence reflects the number of stomachs in which a particular prey group was observed; prey number reflects the total number of prey found;mass reflects the total prey mass of that prey category and %IRI indicates the relative importance of a prey group in the diet.

OCCURRENCE PREY NUMBER MASS %IRI # % # % mg % Plant/unidentifiable 18 69.23 Nematoda 2 7.69 Gastropoda 1 3.85 2 3.23 3.61 1.99 0.85 Isopoda 1 3.85 8 12.90 2.00 1.10 2.26 Chilopoda 1 3.85 3 4.84 1.70 0.94 0.93 Insecta 4 15.38 4 6.45 0.55 0.30 4.35 Coleoptera (adult) 5 19.23 10 16.13 2.34 1.29 14.03 Coleoptera (larval) 1 15.38 12 19.35 46.90 25.81 29.55 Dictyoptera 1 3.85 2 3.23 3.14 1.73 0.81 Diptera (larval) 3 11.54 11 17.74 0.99 0.54 8.82 Ephemeroptera (larval) 1 3.85 1 1.61 0.26 0.14 0.28 Lepidoptera (larval) 2 7.69 2 3.23 66.51 36.60 13.17 Odonata (larval) 2 7.69 3 4.84 7.74 4.26 2.97 Teleostei 4 15.38 4 6.45 45.97 25.30 20.92

Fig. 1. – Pictures in dorsal view of the heads of Clariallabes melas (left) and C. longicauda (right). Indicated are the outlines of the jaw adductors, head width and neurocranial width. Note the more robust appearance of the head in C. longicauda compared to C. melas. 16 Marisa Wyckmans, Anthony Herrel & Dominique Adriaens

Diet in Clariallabes melas DISCUSSION

Twenty (43.5%) of the 46 stomachs examined Our data on cranial morphometrics for a size were empty and 13 (28.3%) contained only range of Clariallabes melas indicate that the jaw unidentifiable or plant matter. The content of adductors become disproportionately bigger as the remaining 13 stomachs could be identified, fish grow; a phenomenon that was previously although these also regularly contained also observed for C. longicauda but is distinctly some unidentifiable or plant matter, which different from growth patterns observed for the was probably accidentally ingested. Table 2 non-hypertrophied Clarias gariepinus (Herrel summarizes the results of the stomach content et al., 2005). Interestingly, and in contrast to the analysis. The most important prey groups for patterns observed for C. longicauda (Wyckmans C. melas are larval specimens of Coleoptera et al., 2007), jaw width and hyoid width within (%IRI=29.6), fish (%IRI =20.9), adult specimens C. melas showed a negative allometry indicating of Coleoptera (%IRI=14.0) and larval specimens that the heads in the large fish are characterized of Lepidoptera (% IRI=9.1). Over 30% of by large jaw muscles but relatively narrow jaws the preys retrieved from the stomachs were and hyoids. Why this is the case currently remains large (over 20mm in length). All hard-shelled unclear, but we suggest that the relatively narrow prey retrieved from the stomachs had been hyoid may allow for a greater ventral excursion effectively crushed, as was observed previously of the mouth floor due to rotation of the hyoid. for C. longicauda (Wyckmans et al., 2007). All else being equal, rotation of a hyoid of a Throughout ontogeny no changes in diet, or in given length characterized by hyoid bars being the relationships between morphology and diet, closer together, as observed here for C. melas, could be demonstrated for C. melas. will result in a greater ventral excursion of the

Fig. 2. – To the left a ventral view x-ray of the head of a Clariallabes melas is shown. On the X-ray the landmarks used to quantify head and jaw dimensions are indicated. To the right a dorsal view picture of a cleared and stained C. melas specimen is shown to illustrate the size of the jaw adductors. Note that the lower jaw and hyoid are not present in this specimen. (1) Lower jaw symphysis; (2, 3) caudal tips of the lower jaw; (4) hyoid symphysis; (5, 6) caudal tips of the hyoid; (7, 8) left and right pectoral fin articulation. Head shape and diet in Clarriallabes 17

Fig. 3. – Scatterplot illustrating the differences in head width between Clariallabes melas and C. longicauda. For a given body size (standard length) C. melas has a significantly narrower head thanC. longicauda.

mouth floor. Previously published kinematic Interestingly, our data indicate clear differences data on suction feeding in clariid catfish with in morphology between the two Clariallabes enlarged jaw adductors (including Clariallabes) species studied here. Even though C. melas is do indeed suggest that the expansion of the on average slightly larger than C. longicauda buccal cavity is largely restricted to a ventrad its head is clearly smaller and the jaw adductors rotation of the hyoid (Van Wassenbergh et are less developed for a given body size (Figs al., 2004, 2006b;c) and consequently larger 1; 3). Although it is tempting to speculate about fish are expected to have an improved suction the ecological significance of this difference performance. An improvement of suction in morphology, our data for C. melas are performance with size has been suggested insufficient to address this in a quantitative previously also for Clarias gariepinus (Van manner. Although the diet in C. longicauda Wassenbergh et al., 2005; 2006d). Although appears more diverse, this may simply be an we suggest that larger C. melas might prey artifact of the small sample size in C. melas. In disproportionately more on relatively large and both species coleopterans and teleost fish are the mobile prey such as teleost fish, our preliminary most important food items with about 60-80% dietary data cannot confirm this. Additional of the individuals having one or the other prey dietary data are clearly needed to shed further in their stomachs. Despite having smaller jaw light on the ecological significance of the adductors, the C. melas examined here crushed observed ontogenetic changes in morphology. all hard prey as evidenced by the crushed 18 Marisa Wyckmans, Anthony Herrel & Dominique Adriaens molluscs, and crushed exoskeletons of insects REFERENCES and other arthropods, similar to the situation reported for C. longicauda (Wyckmans et Aguirre LF, Herrel A, Van Damme R & al., 2007). As many of the prey retrieved from Mathyssen E (2003). The implications of food the stomachs were large (30% over 20mm in hardness for diet in bats. Functional Ecology, length) this suggests an important role for the 17:201-212. hypertrophied jaw adductors. Cabuy E, Adriaens D, Verraes W & Teugels GG (1999). Comparative study on the cranial Our data illustrate how different species of morphology of (Siluriformes: clariid catfish with intermediate jaw adductor Clariidae) and their less anguilliform relatives, hypertrophy may differ dramatically in Clariallabes melas and Clarias gariepinus. morphology and growth. Moreover, and in Journal of Morphology, 240:169-194. contrast to non-specialized suction-feeding Devaere S, Adriaens D, Teugels GG & Verraes catfish such asClarias gariepinus, the growth of W (2005). Morphology and spatial constraints in the head and structures functionally relevant to a dorso-ventrally flattened skull, with a revised feeding is allometric. Although some tendencies species description of Platyallabes tihoni (Poll, for differences in diet can be discerned, these 1944). Journal of Natural History, 39:1653-1673. await further and more robust quantitative analyses. The fact that all hard prey were found Devaere S, Adriaens D, Verraes W & Teugels crushed in the stomachs of the two Clariallabes GG (2001). Cranial morphology of the species is in strong contrast to data for species anguilliform clariid Channallabes apus (Günther, with more extreme jaw adductor hypertrophy 1873) (Teleostei: Siluriformes): are adaptations such as Channalabes or Gymnallabes where related to powerful biting? Journal of Zoology, hard prey are apparently swallowed whole 255:235-250. (Huysentruyt et al., 2004). Thus, whereas Devaere S, Jansen G, Adriaens D & Weekers P the enlarged jaw adductors in these species (2007). Phylogeny of the African representatives with intermediate degrees of jaw specialization of the catfish family Clariidae (Teleostei, appear to provide a performance benefit in Siluriformes) based on a combined analysis: crushing hard prey, this does not appear to be the independent evolution towards anguilliformity. case in more specialized forms. Clearly further Journal of Zoological Systematics and data on morphology and diet in species with Evolutionary Research, 45:214-229. enlarged jaw adductors such as Platyallabes Devaere S, Teugels GG, Adriaens D, tihoni (Devaere et al., 2005), Dolichallabes Huysentruyt F & Verraes W (2004). microphtalmus (Devaere et al., 2004) and their Redescription of Dolichallabes microphthalmus non-specialized sister taxa (Devaere et al., (Poll, 1942) (Siluriformes, Clariidae). Copeia, 2007) will be crucial to quantitatively test for 2004:108-115. evolutionary associations between morphology Grubich J (2003). Morphological convergence and diet in the group. of pharyngeal jaw structure in durophagous perciform fish. Biological Journal of the Linnean Society, 80:147-165. ACKNOWLEDGEMENTS Hernandez LP & Motta PJ (1997). Trophic We would like to thank M. Parrent and J. consequences of differential performance: Snoeks from the RMCA, Tervuren, Belgium ontogeny of oral jaw crushing performance in for the loan of the fish used in this study. This the sheepshead, Archosargus probatocephalus study was supported by grants from the special (Teleostei: Sparidae): Journal of Zoology, research fund from the University of Antwerp and 243:737-756. a Research Programme of the Fund for Scientific Herrel A, McBrayer LD & Larson PM (2007b). Research - Flanders, Belgium (FWO-Vl). Functional basis for intersexual differences in bite Head shape and diet in Clarriallabes 19

force in the lizard Anolis carolinensis. Biological of the Royal Society London B., 271:2501-2508. Journal of the Linnean Society, 91:111-119. Lappin AK & Husak JF (2005). Weapon Herrel A, Adriaens D, Verraes W & Aerts P performance, not size, determines mating (2002). Bite performance in clariid fishes with success and potential reproductive output in the hypertrophied jaw adductors as deduced by bite collared lizard (Crotaphytus collaris). American modeling. Journal of Morphology, 235:196-205. Naturalist, 166:426-436. Herrel A, Schaerlaeken V, Meyers JJ, Metzger Lauder GV (1983). Neuromuscular patterns and the KA & Ross CA (2007a). The evolution of origin of trophic specialization in fishes. Science, cranial design and performance in squamates: 219:1235-1237. consequences of skull-bone reduction on feeding Mittelbach GG, Osenberg CW & Wainwright behavior. Integrative and Comparative Biology, PC (1999). Variation in feeding morphology 47:107-117. between pumpkinseed populations: phenotypic Herrel A, Van Wassenbergh S, Wouters S, plasticity or evolution? Evolutionary Ecology Adriaens D & Aerts P (2005). A functional Research, 1:111-128. morphological approach to the scaling of the Rohlf FJ (2004). tpsDIG32 version 1.40. Available feeding system in the African catfish, Clarias at http://life.bio.sunysb.edu/morph/index.html gariepinus. Journal of Experimental Biology, Sokal RF & Rohlf FJ (1995). Biometry. WH 208:2091-2102. Freeman, New York. Huber DR, Claes JM, Mallefet J & Herrel Streelman JT & Albertson RC (2006). Evolution A (2009). Is extreme bite performance of Novelty in the Cichlid Dentition. Journal of associated with extreme morphologies in sharks. Experimental Zoology, 306B:216-26. Physiological and Biochemical Zoology, 82:20- Turingan RG, Wainwright PC & Hensley DA 28. (1995). Interpopulational variation in prey use and Huyghe K, Vanhooydonck B, Scheers H, feeding biomechanics in Caribbean triggerfishes. Molina-Borja M & Van Damme R (2005). Oecologia, 102:296-304. Morphology, performance and fighting capacity Van Daele PAAG, Herrel A & Adriaens D (2009). in male lizards, Gallotia galloti. Functional Biting performance in teeth-digging African Ecology, 19:800-807. mole-rats (Fukomys, Bathyergidae, Rodentia). Huysentruyt F, Adriaens D, Teugels GG, Physiological and Biochemical Zoology, 82:40- Devaere S, Herrel A, Verraes W & Aerts 50. P (2004). Diet composition in relation to Van Wassenbergh S, Aerts P & Herrel A morphology in some African anguilliform clariid (2005). Scaling of suction-feeding kinematics . Belgian Journal of Zoology, 134:41-46. and dynamics in the African catfish, Clarias Jansen G, Devaere S, Weekers PHH & Adriaens gariepinus. Journal of Experimental Biology, D (2006). Phylogenetic relationships and 208:2103–2114. divergence time estimate of African anguilliform Van Wassenbergh S, Aerts P & Herrel A catfish (Siluriformes: Clariidae) inferred from (2006d). Scaling of suction feeding performance ribosomal gene and spacer sequences. Molecular in the catfish Clarias gariepinus. Physiological Phylogenetics and Evolution, 38:65-78. and Biochemical Zoology, 79:43-56. Korff WL & Wainwright PC (2004). Motor Van Wassenbergh S, Herrel A, Adriaens D pattern control for increasing crushing force in & Aerts P (2004). Effects of jaw adductor the striped burrfish (Chilomycterus schoepfi). hypertrophy on buccal expansions during feeding Zoology, 107:335-346. of air breeding catfishes (Teleostei, Clariidae). Lailvaux SP, Herrel A, Vanhooydonck B, Zoomorphology, 123:81-93. Meyers JJ & Irschick DJ (2004). Fighting tactics Van Wassenbergh S, Herrel A, Adriaens D & differ in two distinct male phenotypes in a lizard: Aerts P (2006b). Modulation and variability of Heavyweight and lightweight bouts. Proceedings 20 Marisa Wyckmans, Anthony Herrel & Dominique Adriaens

prey capture kinematics in clariid catfishes Journal Wyckmans M, Van Wassenbergh S, Adriaens of Experimental Zoology, 305A:559-569. D, Van Damme R & Herrel A (2007). Size- Van Wassenbergh S, Herrel A, Adriaens D & related changes in cranial morphology affect diet Aerts P (2006c). No trade-off between biting and in the catfish Clariallabes longicauda. Biological suction feeding performance in clariid catfish. Journal of the Linnean Society, 92:323-334. Journal of Experimental Biology, 210:27-36. Van Wassenbergh S, Herrel A, Adriaens D, Huysentruyt F, Devaere S & Aerts P (2006a). Received: September 8th, 2010 A catfish that can strike its prey on land. Nature, 440:881. Accepted: May 18th, 2011 Wainwright PC (1987). Biomechanical limits to Branch editor: Schön Isa ecological performance: mollusc-crushing by the Caribbean hogfish, Lachnolaimus maximus (Labridae). Journal of Zoology, 213:283-297.